Abstract
High ambient temperature is a major problem in commercial broiler production in the humid tropics because high producing broiler birds consume more feed, have higher metabolic activity, and thus higher body heat production. To evaluate the effects of two previously isolated potential probiotic strains (Lactobacillus pentosus ITA23 and Lactobacillus acidophilus ITA44) on broilers growing under heat stress condition, a total of 192 chicks were randomly allocated into four treatment groups of 48 chickens each as follows: CL, birds fed with basal diet raised in 24 °C; PL, birds fed with basal diet plus 0.1 % probiotic mixture raised in 24 °C; CH, birds fed with basal diet raised in 35 °C; and PH, birds fed with basal diet plus 0.1 % probiotic mixture raised in 35 °C. The effects of probiotic mixture on the performance, expression of nutrient absorption genes of the small intestine, volatile fatty acids (VFA) and microbial population of cecal contents, antioxidant capacity of liver, and fatty acid composition of breast muscle were investigated. Results showed that probiotic positively affected the final body weight under both temperature conditions (PL and PH groups) compared to their respective control groups (CL and CH). Probiotic supplementation numerically improved the average daily gain (ADG) under lower temperature, but significantly improved ADG under the higher temperature (P < 0.05) by sustaining high feed intake. Under the lower temperature environment, supplementation of the two Lactobacillus strains significantly increased the expression of the four sugar transporter genes tested (GLUT2, GLUT5, SGLT1, and SGLT4) indicating probiotic enhances the absorption of this nutrient. Similar but less pronounced effect was also observed under higher temperature (35 °C) condition. In addition, the probiotic mixture improved bacterial population of the cecal contents, by increasing beneficial bacteria and decreasing Escherichia coli population, which could be because of higher production of VFA in the cecum, especially at heat stress condition. The two Lactobacillus strains also improved the fatty acid profile of meat, including at heat stress. Generally, the two Lactobacillus strains can be considered as good potential probiotics for chickens due to their good probiotic properties and remarkable efficacy on broiler chickens.
Similar content being viewed by others
References
Abdel-Rahman H, Shawky S, Ouda H, Nafeaa A, Orabi S (2013) Effect of two probiotics and bioflavonoids supplementation to the broilers diet and drinking water on the growth performance and hepatic antioxidant parameters. Global Vet 10:734–741
Adibi SA (1997) The oligopeptide transporter (Pept-1) in human intestine: biology and function. Gastroenterology 113:332–340
Alkhalf A, Alhaj M, Al-Homidan I (2010) Influence of probiotic supplementation on blood parameters and growth performance in broiler chickens. Saudi J Biol Sci 17:219–225
Altaher YW, Jahromi MF, Ebrahim R, Zulkifli I, Liang JB (2015) Lactobacillus pentosus ITA23 and L. acidipiscis ITA44 enhance feed conversion efficiency and beneficial gut microbiota in broiler chickens. Braz J Poult Sci 17:159–164
Aluwong T, Kawu M, Raji M, Dzenda T, Govwang F, Sinkalu V, et al. (2013) Effect of yeast probiotic on growth, antioxidant enzyme activities and malondialdehyde concentration of broiler chickens. Antioxidants 2:326–339
Amaretti A, di Nunzio M, Pompei A, Raimondi S, Rossi M, Bordoni A (2013) Antioxidant properties of potentially probiotic bacteria: in vitro and in vivo activities. Appl Microbiol Biotechnol 97:809–817
Argyri AA, Zoumpopoulou G, Karatzas K-AG, Tsakalidou E, Nychas G-JE, Panagou EZ, et al. (2013) Selection of potential probiotic lactic acid bacteria from fermented olives by in vitro tests. Food Microbiol 33:282–291
Benzie IFF, Strain JJ (1996) The ferric reducing ability of plasma (FRAP) as a measure of “antioxidant power”: the FRAP assay. Anal Biochem 239:70–76
Bitterncourt LC, CCd S, PDSR G, DCZ D, Rd A, Araújo LF (2011) Influence of a probiotic on broiler performance. Rev Bras Zootecn 40:2739–2743
Capcarova M, Weiss J, Hrncar C, Kolesarova A, Pal G (2010) Effect of Lactobacillus fermentum and Enterococcus faecium strains on internal milieu, antioxidant status and body weight of broiler chickens. J Anim Physiol Anim Nutr 94:215–224
Caplice E, Fitzgerald GF (1999) Food fermentations: role of microorganisms in food production and preservation. Int J Food Microbiol 50:131–149
Cieslak A, Zmora P, Pers-Kamczyc E, Szumacher-Strabel M (2012) Effects of tannins source (vaccinium vitis idaea L.) on rumen microbial fermentation in vivo. Anim Feed Sci Technol 176:102–106
Collins J, Thornton G, Sullivan G (1998) Selection of probiotic strains for human applications. Int Dairy J 8:487–490
De Vuyst L, Leroy F (2007) Bacteriocins from lactic acid bacteria: production, purification, and food applications. J Mol Microbiol Biotechnol 13:194–199
Dhama K, Latheef SK, Saminathan M, Abdul Samad H, Karthik K, Tiwari R, Khan RU, Alagawany M, Farag MR, Alam GM, Laudadio V, Tufarelli V (2015) Multiple beneficial applications and modes of action of herbs in poultry health and production—a review. Int J Pharmacol 11:152–176
Ebrahimi M, Rajion M, Goh Y, Sazili A (2012) Impact of different inclusion levels of oil palm (Elaeis guineensis Jacq.) fronds on fatty acid profiles of goat muscles. J Anim Physiol Anim Nutr 96:962–969
Ebrahimi R, Jahromi MF, Liang JB, Soleimani AF, Shokryazdan P, Idrus Z (2015) Effect of dietary lead on intestinal nutrient transporters mRNA expression in broiler chickens. BioMed Research Int. doi:10.1155/2015/149745
EC Regulation No. 1831/2003 of European Parliament and the Council of 22 September 2003 on additives for use in animal nutrition. Off. J. Eur. Union. Page L268/36 in OJEU of 10/18/2003. Brussels,0020Belgium, 2003
Fdr L, De Vuyst L (2004) Lactic acid bacteria as functional starter cultures for the food fermentation industry. Trends Food Sci Technol 15:67–78
Folch J, Lees M, Sloane-Stanley GH (1957) A simple method for the isolation and purification of total lipids from animal tissues. J Biol Chem 226:497–509
Fuller R (ed) (1992) Probiotics: the scientific basis. Chapman & Hall Ltd., London
Garriga C, Hunter RR, Amat C, Planas JM, Mitchell MA, Moretó M (2006) Heat stress increases apical glucose transport in the chicken jejunum. Am J Physiol-Reg Int Comp Physiol 290:195–201
Gilbert ER, Li H, Emmerson DA, Webb KE, Wong EA (2007) Developmental regulation of nutrient transporter and enzyme mRNA abundance in the small intestine of broilers. Poult Sci 86:1739–1753
Halliwell B, Gutteridge JMC (1984) Oxygen toxicity, oxygen radicals, transition metals and disease. Biochem J 219:1–14
Halliwell B, JMC G (1989) Free radicals in biology and medicine. Clarendon Press, Oxford
Herzallah S (2013) Enrichment of conjugated linoleic acid (CLA) in hen eggs and broiler chickens meat by lactic acid bacteria. Br Poult Sci 54:747–752
Huang D, Ou B, Ronald L (2003) The chemistry behind antioxidant capacity assays. J Agr Food Chem 53:1841–1856
Jain S, Yadav H, Ravindra Sinha P (2009) Antioxidant and cholesterol assimilation activities of selected lactobacilli and lactococci cultures. J Dairy Res 76:385–391
Kalavathy R, Abdullah N, Jalaludin S, Wong M, Ho YW (2006) Effects of Lactobacillus feed supplementation on cholesterol, fat content and fatty acid composition of the liver, muscle and carcass of broiler chickens. Anim Res 55:77–82
Khan RU, Naz S, Nikousefat Z, Tufarelli V, Laudadio V (2012) Thymus vulgaris: alternative to antibiotics in poultry feed. World Poult Sci J 68:401–408
Kim CJ, Namkung H, An MS, Paik IK (1988) Supplementation of probiotics to broiler diets containing moldy corn. Korean J Anim Sci 30:542–548
Klayraung S, Okonogi S (2009) Antibacterial and antioxidant activities of acid and bile resistant strains of Lactobacillus fermentum isolated from Miang. Braz J Microbiol 40757-766
Lan PTN, Sakamoto M, Benno Y (2004) Effects of two probiotic Lactobacillus strains on jejunal and cecal microbiota of broiler chicken under acute heat stress condition as revealed by molecular analysis of 16S rRNA genes. Microbiol Immunol 48:917–929
Li S, Zhao Y, Zhang L, Zhang X, Huang L, Li D, et al. (2012) Antioxidant activity of Lactobacillus plantarum strains isolated from traditional Chinese fermented foods. Food Chem 135:1914–1919
Liao X, Wu R, Ma G, Zhao L, Zheng Z, Zhang R (2015) Effects of Clostridium butyricum on antioxidant properties, meat quality and fatty acid composition of broiler birds. Lipids Health Dis 14:36–45
Lin MY, Chang FJ (2000) Antioxidative effect of intestinal bacteria Bifidobacterium longum ATCC 15708 and Lactobacillus acidophilus ATCC 4356. Dig Dis Sci 45:1617–1622
Mohan B, Kadirvel R, Natarajan A, Bhaskaran M (1996) Effect of probiotic supplementation on growth, nitrogen utilisation and serum cholesterol in broilers. Br Poult Sci 37:395–401
Mountzouris KC, Tsirtsikos P, Kalamara E, Nitsch S, Schatzmayr G, Fegeros K (2007) Evaluation of the efficacy of a probiotic containing Lactobacillus, Bifidobacterium, Enterococcus, and Pediococcus strains in promoting broiler performance and modulating cecal microflora composition and metabolic activities. Poult Sci 86:309–317
Muller L, Frohlich K, Bohm V (2011) Comparative antioxidant activities of carotenoids measured by ferric reducing antioxidant power (FRAP), ABTS bleaching assay (αTEAC), DPPH assay and peroxyl radical scavenging assay. Food Chem 129:139–148
Navidshad B, Liang JB, Jahromi MF (2012) Correlation coefficients between different methods of expressing bacterial quantification using real time PCR. Int J Mol Sci 13:2119–2132
Neal-McKinney JM, Lu X, Duong T, Larson CL, Call DR, Shah DH, et al. (2012) Production of organic acids by probiotic lactobacilli can be used to reduce pathogen load in poultry. PLoS One 7:e43928
NRC (1994) Nutrient requirements of poultry. National Research Council, Washington DC
Ramasamy K, Abdullah N, Jalaludin S, Wong M, Ho YW (2009) Effects of Lactobacillus cultures on performance of laying hens, and total cholesterol, lipid and fatty acid composition of egg yolk. J Sci Food Agric 89:482–486
Ramasamy K, Abdullah N, Jalaludin S, Wong MC, Ho YW (2006) Effects of Lactobacillus feed supplementation on cholesterol, fat content and fatty acid composition of the liver, muscle and carcass of broiler chickens. Anim Res 55:77–82
Saleh AA (2014) Effect of dietary mixture of Aspergillus probiotic and selenium nano-particles on growth, nutrient digestibilities, selected blood parameters and muscle fatty acid profile in broiler chickens. Anim Sci Pap Rep 32:65–79
Saleh AA, Eid YZ, Ebeid TA, Amber K, Kamizono T, Ohtsuka A, et al (2011) Aspergillus awamori as probiotic in broiler chickens. In Proceedings of the 9th Asia Pacific Poultry Conference, Taipei, Taiwan
Salma U, Miah A, Maki T, Nishimura M, Tsujii H (2007) Effect of dietary Rhodobacter capsulatus on cholesterol concentration and fatty acid composition in broiler meat. Poult Sci 86:1920–1926
Saulnier D, Spinler JK, Gibson GR, Versalovic J (2009) Mechanisms of probiosis and prebiosis: considerations for enhanced functional foods. Current Opinion in Biotechnology. 20:135–141
Shen X, Yi D, Ni X, Zeng D, Jing B, Lei M, et al. (2014) Effects of Lactobacillus plantarum on production performance, immune characteristics, antioxidant status, and intestinal microflora of bursin-immunized broilers. Can J Microbiol 60:193–202
Shokryazdan P (2013) Characterization and exploitation of Lactobacillus strains as potential probiotics for humans and chickens. PhD Thesis, Universiti Putra Malaysia
Shokryazdan P, Kalavathy R, Sieo CC, Alitheen NB, Liang JB, Jahromi MF, et al. (2014a) Isolation and characterization of Lactobacillus strains as potential probiotics for chickens. Pertanika J Trop Agric Sci 37:141–157
Shokryazdan P, Liang JB, Jahromi MF, Abdullah N (2015) Probiotic potential of lactic acid bacteria isolated from mulberry silage. J Pure Appl Microbiol(In press)
Shokryazdan P, Sieo CC, Kalavathy R, Liang JB, Alitheen NB, Faseleh Jahromi M, et al (2014b) Probiotic potential of Lactobacillus strains with antimicrobial activity against some human pathogenic strains. Biomed Res Int Article ID 927268, DOI:0.1155/2014/927268
Soomro A, Masud T, Anwaar K (2002) Role of lactic acid bacteria (LAB) in food preservation and human health—a review. Pak J Nutr 1:20–24
Suskovic J, Blazenka K, Beganovic J, Pavunc AL, Habjanic K, Matosic S (2010) Antimicrobial activity—the most important property of probiotic and starter lactic acid bacteria. Food Technol Biotechnol 48:296–307
Tarun M (2008) Growth performance of broilers fed with different strains of probiotics. 16th IFOAM Organic World Congress. Modena, Italy. Available at http://orgprints.org/11625
Timmerman HM, Veldman A, Van den Elsen E, Rombouts FM, Beynen AC (2006) Mortality and growth performance of broilers given drinking water supplemented with chicken-specific probiotics. Poult Sci 85:1383–1388
Tsai JC, Huang GJ, Chiu TH, Huang SS, Huang SC, Huang TH, et al. (2011) Antioxidant activities of phenolic components from various plants of Desmodium species. Afr J Pharm Pharmacol 5:468–476
Tufarelli V, Dario M, Laudadio V (2007) Effect of xylanase supplementation and particle-size on performance of guinea fowl broilers fed wheat-based diets. Int J Poult Sci 4:302–307
Uldry M, Thorens B (2004) The SLC2 family of facilitated hexose and polyol transporters. Pflugers Arch 447:480–489
Vicente JL, Aviña L, Torres-Rodriguez A, Hargis B, Tellez G (2007) Effect of a Lactobacillus spp-based probiotic culture product on broiler chicks performance under commercial conditions. Int J Poult Sci 6:154–156
van der Wielen PW, Biesterveld S, Notermans S, Hofstra H, Urlings BA, van Knapen F (2000) Role of volatile fatty acids in development of the cecal microflora in broiler chickens during growth. Appl Environ Microbiol 66:2536–2540
Wright EM, Turk E (2004) The sodium/glucose cotransport family SLC5. Pflugers Arch 447:510–518
Yeo J, Kim K (1997) Effect of feeding diets containing an antibiotic, a probiotic, or yucca extract on growth and intestinal urease activity in broiler chicks. Poult Sci 76:381–385
Zerangue N, Kavanaugh MP (1996) Flux coupling in a neuronal glutamate transporter. Nature 383:634–637
Acknowledgments
This study was supported by the LRGS Fasa 1/2012 (Universiti Putra Malaysia) provided by the Ministry of Education Malaysia.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no competing interests.
Rights and permissions
About this article
Cite this article
Faseleh Jahromi, M., Wesam Altaher, Y., Shokryazdan, P. et al. Dietary supplementation of a mixture of Lactobacillus strains enhances performance of broiler chickens raised under heat stress conditions. Int J Biometeorol 60, 1099–1110 (2016). https://doi.org/10.1007/s00484-015-1103-x
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00484-015-1103-x